Glycolysis is independent of oxygenation state in stimulated human skeletal muscle <i>in vivo</i>

Conley, Kevin E.; Kushmerick, Martin J.; Jubrias, Sharon A.

doi:10.1111/j.1469-7793.1998.935bg.x

Cited by 86 publications

(104 citation statements)

References 31 publications

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“…These three types of cell intermingle in a muscle, so that lactate as a final product of type IIb fiber is transported to type I and type IIa myocytes and used as a fuel for oxidative phosphorylation. These processes are independent of oxygen status (75), clarifying the long-acknowledged phenomenon of 'lactate threshold' or 'anaerobic threshold' (76). The known recruitment order from slow-twitch to larger fast-twitch motor units means that their consideration must be given in an experimental design.…”

Section: Anaerobic Glycolysismentioning

confidence: 99%

Skeletal muscle energetics with PNMR: personal views and historic perspectives

Chance

Nioka

et al. 2006

NMR in Biomedicine

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This article reviews historical and current NMR approaches to describing in vivo bioenergetics of skeletal muscles in normal and diseased populations. It draws upon the first author's more than 70 years of personal experience in enzyme kinetics and the last author's physiological approaches. The development of in vivo PNMR jointly with researchers around the world is described. It is explained how non-invasive PNMR has advanced human exercise biochemistry, physiology and pathology. Further, after a brief explanation of bioenergetics with PNMR on creatine kinase, anerobic glycolysis and mitochondrial oxidative phosphorylation, some basic and controversial subjects are focused upon, and the authors' view of the subjects are offered, with questions and answers. Some of the research has been introduced in exercise physiology. Future directions of NMR on bioenergetics, as a part of system biological approaches, are indicated.

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Section: Anaerobic Glycolysismentioning

confidence: 99%

Skeletal muscle energetics with PNMR: personal views and historic perspectives

Chance

Nioka

et al. 2006

NMR in Biomedicine

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“…Because the shortfall in the ATP balance is met by the glycolytic flux in anoxia, these results also suggest that glycolytic flux is independent of oxygenation state. Our previous noninvasive 31 P MR spectroscopy measurements in human muscle showed similar glycolytic flux under anoxic and aerobic exercise conditions (9). This glycolytic flux exceeded the oxidation of pyruvate, as shown by the accumulation of H ϩ and the decrease of pH during contraction.…”

Section: Discussionmentioning

confidence: 96%

“…This apparently ''excessive'' glycolytic flux is not restricted to rattling; Fig. 5 shows that glycolysis exceeds oxidative needs in three human muscles during sustained contractions as well (9,14,34). The fate of this lactate seems to be primarily uptake by other muscles, because both heart and skeletal muscle readily take up and oxidize circulating lactate (35,36).…”

Section: Discussionmentioning

confidence: 99%

“…New magnetic resonance (MR) techniques for partitioning intracellular ATP supply in vivo permitted this comparison in human muscles and were used to show that glycolytic flux is independent of O 2 state (9). The similarities of flux under anoxia and aerobic conditions in that study indicated that glycolysis is not mutually exclusive with oxidative phosphorylation.…”

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confidence: 98%

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From the Cover: Shaking up glycolysis: Sustained, high lactate flux during aerobic rattling

Kemper

Lindstedt

Hartzler

et al. 2000

Proceedings of the National Academy of Sciences

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Substantial ATP supply by glycolysis is thought to reflect cellular anoxia in vertebrate muscle. An alternative hypothesis is that the lactate generated during contraction reflects sustained glycolytic ATP supply under well-oxygenated conditions. We distinguished these hypotheses by comparing intracellular glycolysis during anoxia to lactate efflux from muscle during sustained, aerobic contractions. We examined the tailshaker muscle of the rattlesnake because of its uniform cell properties, exclusive blood circulation, and ability to sustain rattling for prolonged periods. Here we show that glycolysis is independent of the O 2 level and supplies one-third of the high ATP demands of sustained tailshaking. Fatigue is avoided by rapid H ؉ and lactate efflux resulting from blood flow rates that are among the highest reported for vertebrate muscle. These results reject the hypothesis that glycolysis necessarily reflects cellular anoxia. Instead, they demonstrate that glycolysis can provide a high and sustainable supply of ATP along with oxidative phosphorylation without muscle fatigue.31 P magnetic resonance spectroscopy ͉ high-energy phosphates ͉ rattlesnake L actate generation by tissues is often taken as a sign of tissue hypoxia (1). This thinking has led to the anaerobic threshold hypothesis, which links lactate generation in exercising muscle to an intracellular O 2 limitation to respiration of pyruvate (2). However, many tissues seem to generate lactate under aerobic conditions (so-called aerobic glycolysis) in a process linking glycolytic ATP supply to ion transport (3-5). For example, lactate generation by muscles exercising at rates well below their aerobic maximum (6) supports this alternative explanation. Muscle PO 2 seems to be well above limits to mitochondrial respiration in these muscles as indicated by indirect measures of tissue oxygenation involving myoglobin saturation (6, 7). This finding questions an O 2 limit to respiration as the basis for lactate generation in exercising muscle. However, these indirect measures do not have the spatial resolution to determine intracellular PO 2 to rule out local tissue anoxia (8).A definitive test of whether an O 2 limitation is responsible for lactate generation during sustained contractions is possible by using a direct comparison of glycolysis during anoxic and sustained aerobic contractions. New magnetic resonance (MR) techniques for partitioning intracellular ATP supply in vivo permitted this comparison in human muscles and were used to show that glycolytic flux is independent of O 2 state (9). The similarities of flux under anoxia and aerobic conditions in that study indicated that glycolysis is not mutually exclusive with oxidative phosphorylation. This glycolytic flux should generate a high lactate efflux into the blood during aerobic contractions and serves as a test for MR results. The rattlesnake tailshaker muscles are well suited for a direct comparison of intracellular glycolysis to lactate efflux. First, the uniform muscle fiber properties (10, 11...

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“…A previous study reported that muscle activation (Blei et al 1993) and contractile cost per twitch (Conley et al 1998) were unchanged during muscle contraction under ischemic and aerobic conditions. In the human forearm muscle during isometric exercise at three intensities, there were no significant differences in the sum of ATP production rates between Intramuscular O 2 -Ex and Anaero-Ex.…”

Section: The Contribution Of Intramuscular Oxidative Metabolism To Tomentioning

confidence: 99%

Contribution of Intramuscular Oxidative Metabolism to Total ATP Production during Forearm Isometric Exercise at Varying Intensities

Kimura

Hamaoka²,

Kurosawa

et al. 2006

Tohoku J. Exp. Med.

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It is not fully clear whether intramuscular oxidative metabolism contributes to total adenosine triphosphate (ATP) production during forearm isometric exercise at varying intensities. We tested hypothesis that oxidative metabolism with intramuscular O 2 contributes to lessen the dependence on anaerobic metabolism, in particular phosphocreatine (PCr) breakdown. Seven male subjects were tested for changes in muscle oxygenation (MO 2 ) and highenergy phosphates in forearm flexor muscles at rest and during exercise under arterial occlusion by 31-phosphorus magnetic resonance spectroscopy ( 31 P-MRS) and near infrared spectroscopy (NIRS). Isometric wrist flexion exercise was performed for 1 min or until exhaustion at intensities corresponding to 30%, 50% and 70% of maximal voluntary contraction (MVC) under intramuscular O 2 (Intramuscular O 2 -Ex) and anaerobic (Anaero-Ex) conditions. Oxidative ATP production in Intramuscular O 2 -Ex was calculated as 0.05 ± 0.01 mM/s for 30%MVC, 0.08 ± 0.01 mM/s for 50%MVC and 0.11 ± 0.01 mM/s for 70%MVC. At a lower intensity (30%MVC), PCr breakdown rate (0.17 ± 0.02 mM/s) of Anaero-Ex was significantly higher than the rate (0.13 ± 0.01 mM/s) of Intramuscular O 2 -Ex ( p < 0.05). There was no significant difference in ATP production rates through PCr breakdown and glycolysis between Intramuscular O 2 -Ex and Anaero-Ex at the higher intensities (50% and 70%MVC). In conclusion, intramuscular oxidative metabolism plays a significant role in reducing the dependence on PCr breakdown during isometric exercise at a lower intensity (30%MVC).intramuscular O 2 ; oxidative metabolism; PCr breakdown

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Glycolysis is independent of oxygenation state in stimulated human skeletal muscle in vivo

Cited by 86 publications

References 31 publications

Skeletal muscle energetics with PNMR: personal views and historic perspectives

Skeletal muscle energetics with PNMR: personal views and historic perspectives

From the Cover: Shaking up glycolysis: Sustained, high lactate flux during aerobic rattling

Contribution of Intramuscular Oxidative Metabolism to Total ATP Production during Forearm Isometric Exercise at Varying Intensities

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